Grooming site preferences in black capuchin monkeys: Hygienic vs. social functions revisited.

When primates groom each other, they tend to concentrate on those parts of the body they cannot efficiently self-groom (i.e., not visually accessible), and prefer to intensify grooming in areas with high hair density, thus suggesting a hygienic function. However, preferences for some body sites over others during social grooming may also result from different degrees of social bonding and relative dominance. To assess the relative importance of physical (hygienic) and social factors, we examined grooming interactions in two groups of wild black capuchin monkeys (Sapajus nigritus) during 15 nonconsecutive months. We evaluated the distribution of social grooming across body sites according to their accessibility by self-grooming and hair density. At the same time, we assessed whether the degree of dyadic social bonding affects the relative body orientation between groomer and groomee and the access to vulnerable body sites (e.g., face, throat, groin) during grooming. As expected, capuchins preferentially groomed inaccessible body sites (e.g., back and head), with a disproportionate effort directed to the tufts of their partners. We found that dyadic social bond strength, together with rank distance, significantly affected the proportion of grooming in ventro-ventral body relative orientation only in dominant-subordinate groomer-groomee dyads. This may indicate that, when two individuals differ in rank but are strongly bonded, the level of uncertainty related to the social context is already resolved and thus grooming per se is no longer perceived by the subordinate as an uncertain/risky situation. We found no effect of social bonding on grooming vulnerable body sites for any type of dyad. Our findings suggest that grooming site preferences in black capuchin monkeys simultaneously reflect hygienic and social functions.

ATLANTIC-PRIMATES: a dataset of communities and occurrences of primates in the Atlantic Forests of South America.

Primates play an important role in ecosystem functioning and offer critical insights into human evolution, biology, behavior, and emerging infectious diseases. There are 26 primate species in the Atlantic Forests of South America, 19 of them endemic. We compiled a dataset of 5,472 georeferenced locations of 26 native and 1 introduced primate species, as hybrids in the genera Callithrix and Alouatta. The dataset includes 700 primate communities, 8,121 single species occurrences and 714 estimates of primate population sizes, covering most natural forest types of the tropical and subtropical Atlantic Forest of Brazil, Paraguay and Argentina and some other biomes. On average, primate communities of the Atlantic Forest harbor 2 ± 1 species (range = 1-6). However, about 40% of primate communities contain only one species. Alouatta guariba (N = 2,188 records) and Sapajus nigritus (N = 1,127) were the species with the most records. Callicebus barbarabrownae (N = 35), Leontopithecus caissara (N = 38), and Sapajus libidinosus (N = 41) were the species with the least records. Recorded primate densities varied from 0.004 individuals/km2 (Alouatta guariba at Fragmento do Bugre, Paraná, Brazil) to 400 individuals/km2 (Alouatta caraya in Santiago, Rio Grande do Sul, Brazil). Our dataset reflects disparity between the numerous primate census conducted in the Atlantic Forest, in contrast to the scarcity of estimates of population sizes and densities. With these data, researchers can develop different macroecological and regional level studies, focusing on communities, populations, species co-occurrence and distribution patterns. Moreover, the data can also be used to assess the consequences of fragmentation, defaunation, and disease outbreaks on different ecological processes, such as trophic cascades, species invasion or extinction, and community dynamics. There are no copyright restrictions. Please cite this Data Paper when the data are used in publications. We also request that researchers and teachers inform us of how they are using the data.

Effects of human impacts on habitat use, activity patterns and ecological relationships among medium and small felids of the Atlantic Forest.

Competition theory and niche theory suggest that two morphologically similar species may coexist by reducing the overlap of at least one dimension of their ecological niche. The medium and small Neotropical felids are an interesting group of carnivore species for studying intraguild competition. Due to differences in size it is expected that the larger ocelot exert strong interference competition on the smaller felids (southern tiger cat, margay and jaguarundi); which, in turn, may exert exploitative competition among themselves. Moreover, landscape changes due to human activities may alter these interspecific interactions. We studied the habitat use and the spatial and temporal interspecific relations of the medium and small Atlantic Forest felids, in a landscape with different levels of anthropogenic impact. We estimated the detection probability, and occupancy probability of these cats and whether these parameters are affected by environmental and anthropogenic variables or by the estimated occupancy and detection probability of the ocelot. We estimated the overlap in daily activity patterns between pairs of the four species and changes in their activity in response to anthropogenic impact. We also studied the potential changes that may have occurred in the daily activity of the small felids in relation to ocelot's occupancy probability. The probability of habitat use of the small- and medium-size felids was negatively associated to the intensity of landscape use by humans. Co-occurrence models indicated that the probability of habitat use by southern tiger cats decreased with ocelot occupancy probability. This effect was higher as human disturbance increased. Moreover, the ocelot and the southern tiger cat became more nocturnal in sites with higher human access, suggesting that they may be temporally avoiding encounters with humans or dogs. Conservation of medium and small felids in the Atlantic Forest depends not only on the establishment and implementations of protected areas but also on the management of human's land uses.

Ecological correlates of the spatial co-occurrence of sympatric mammalian carnivores worldwide.

The composition of local mammalian carnivore communities has far-reaching effects on terrestrial ecosystems worldwide. To better understand how carnivore communities are structured, we analysed camera trap data for 108 087 trap days across 12 countries spanning five continents. We estimate local probabilities of co-occurrence among 768 species pairs from the order Carnivora and evaluate how shared ecological traits correlate with probabilities of co-occurrence. Within individual study areas, species pairs co-occurred more frequently than expected at random. Co-occurrence probabilities were greatest for species pairs that shared ecological traits including similar body size, temporal activity pattern and diet. However, co-occurrence decreased as compared to other species pairs when the pair included a large-bodied carnivore. Our results suggest that a combination of shared traits and top-down regulation by large carnivores shape local carnivore communities globally.

Experimental testing of reciprocal effects of nutrition and parasitism in wild black capuchin monkeys.

Nutritional stress may predispose individuals to infection, which in turn can have further detrimental effects on physical condition, thus creating an opportunity for reciprocal effects between nutrition and parasitism. Little experimental investigation has been conducted on this "vicious circle" hypothesis in wild animals, especially under natural conditions. We evaluated the reciprocal effects of nutritional status and parasitism using an experimental approach in two groups of wild black capuchin monkeys (Sapajus nigritus). Across two consecutive winters, we collected faecal samples from identified capuchins to determine presence and load of gastrointestinal helminthes, and measured individual body mass as a proxy of physical condition. Food availability was manipulated by provisioning monkeys with bananas, and parasite burdens by applying antiparasitic drugs to selected individuals. We found no effect of antiparasitic drugs on physical condition, but parasite loads decreased in response to high levels of food availability. Our results represent the first experimental evidence that the nutritional status may drive parasite dynamics in a primate.

ATLANTIC-CAMTRAPS: a dataset of medium and large terrestrial mammal communities in the Atlantic Forest of South America.

Our understanding of mammal ecology has always been hindered by the difficulties of observing species in closed tropical forests. Camera trapping has become a major advance for monitoring terrestrial mammals in biodiversity rich ecosystems. Here we compiled one of the largest datasets of inventories of terrestrial mammal communities for the Neotropical region based on camera trapping studies. The dataset comprises 170 surveys of medium to large terrestrial mammals using camera traps conducted in 144 areas by 74 studies, covering six vegetation types of tropical and subtropical Atlantic Forest of South America (Brazil and Argentina), and present data on species composition and richness. The complete dataset comprises 53,438 independent records of 83 species of mammals, includes 10 species of marsupials, 15 rodents, 20 carnivores, eight ungulates and six armadillos. Species richness averaged 13 species (±6.07 SD) per site. Only six species occurred in more than 50% of the sites: the domestic dog Canis familiaris, crab-eating fox Cerdocyon thous, tayra Eira barbara, south American coati Nasua nasua, crab-eating raccoon Procyon cancrivorus and the nine-banded armadillo Dasypus novemcinctus. The information contained in this dataset can be used to understand macroecological patterns of biodiversity, community, and population structure, but also to evaluate the ecological consequences of fragmentation, defaunation, and trophic interactions.

Publish (in English) or perish: The effect on citation rate of using languages other than English in scientific publications.

There is a tendency for non-native English scientists to publish exclusively in English, assuming that this will make their articles more visible and cited. We tested this hypothesis by comparing the effect of language on the number of citations of articles published in six natural sciences journals from five countries that publish papers in either English or other languages. We analyzed the effect of language (English vs non-English), paper length, and year of publication on the number of citations. The articles published in English have a higher number of citations than those published in other languages, when the effect of journal, year of publication, and paper length are statistically controlled. This may result because English articles are accessible to a larger audience, but other factors need to be explored. Universities and scientific institutions should be aware of this situation and improve the teaching of English, especially in the natural sciences.

Space Use and Movement of a Neotropical Top Predator: The Endangered Jaguar.

Accurately estimating home range and understanding movement behavior can provide important information on ecological processes. Advances in data collection and analysis have improved our ability to estimate home range and movement parameters, both of which have the potential to impact species conservation. Fitting continuous-time movement model to data and incorporating the autocorrelated kernel density estimator (AKDE), we investigated range residency of forty-four jaguars fit with GPS collars across five biomes in Brazil and Argentina. We assessed home range and movement parameters of range resident animals and compared AKDE estimates with kernel density estimates (KDE). We accounted for differential space use and movement among individuals, sex, region, and habitat quality. Thirty-three (80%) of collared jaguars were range resident. Home range estimates using AKDE were 1.02 to 4.80 times larger than KDE estimates that did not consider autocorrelation. Males exhibited larger home ranges, more directional movement paths, and a trend towards larger distances traveled per day. Jaguars with the largest home ranges occupied the Atlantic Forest, a biome with high levels of deforestation and high human population density. Our results fill a gap in the knowledge of the species' ecology with an aim towards better conservation of this endangered/critically endangered carnivore-the top predator in the Neotropics.

A biodiversity hotspot losing its top predator: The challenge of jaguar conservation in the Atlantic Forest of South America.

The jaguar is the top predator of the Atlantic Forest (AF), which is a highly threatened biodiversity hotspot that occurs in Brazil, Paraguay and Argentina. By combining data sets from 14 research groups across the region, we determine the population status of the jaguar and propose a spatial prioritization for conservation actions. About 85% of the jaguar's habitat in the AF has been lost and only 7% remains in good condition. Jaguars persist in around 2.8% of the region, and live in very low densities in most of the areas. The population of jaguars in the AF is probably lower than 300 individuals scattered in small sub-populations. We identified seven Jaguar Conservation Units (JCUs) and seven potential JCUs, and only three of these areas may have ≥50 individuals. A connectivity analysis shows that most of the JCUs are isolated. Habitat loss and fragmentation were the major causes for jaguar decline, but human induced mortality is the main threat for the remaining population. We classified areas according to their contribution to jaguar conservation and we recommend management actions for each of them. The methodology in this study could be used for conservation planning of other carnivore species.

Yellow fever impact on brown howler monkeys (Alouatta guariba clamitans) in Argentina: a metamodelling approach based on population viability analysis and epidemiological dynamics

In South America, yellow fever (YF) is an established infectious disease that has been identified outside of its traditional endemic areas, affecting human and nonhuman primate (NHP) populations. In the epidemics that occurred in Argentina between 2007-2009, several outbreaks affecting humans and howler monkeys (Alouatta spp) were reported, highlighting the importance of this disease in the context of conservation medicine and public health policies. Considering the lack of information about YF dynamics in New World NHP, our main goal was to apply modelling tools to better understand YF transmission dynamics among endangered brown howler monkey (Alouatta guariba clamitans) populations in northeastern Argentina. Two complementary modelling tools were used to evaluate brown howler population dynamics in the presence of the disease: Vortex, a stochastic demographic simulation model, and Outbreak, a stochastic disease epidemiology simulation. The baseline model of YF disease epidemiology predicted a very high probability of population decline over the next 100 years. We believe the modelling approach discussed here is a reasonable description of the disease and its effects on the howler monkey population and can be useful to support evidence-based decision-making to guide actions at a regional level.

Yellow fever impact on brown howler monkeys (Alouatta guariba clamitans) in Argentina: a metamodelling approach based on population viability analysis and epidemiological dynamics.

In South America, yellow fever (YF) is an established infectious disease that has been identified outside of its traditional endemic areas, affecting human and nonhuman primate (NHP) populations. In the epidemics that occurred in Argentina between 2007-2009, several outbreaks affecting humans and howler monkeys (Alouatta spp) were reported, highlighting the importance of this disease in the context of conservation medicine and public health policies. Considering the lack of information about YF dynamics in New World NHP, our main goal was to apply modelling tools to better understand YF transmission dynamics among endangered brown howler monkey (Alouatta guariba clamitans) populations in northeastern Argentina. Two complementary modelling tools were used to evaluate brown howler population dynamics in the presence of the disease: Vortex, a stochastic demographic simulation model, and Outbreak, a stochastic disease epidemiology simulation. The baseline model of YF disease epidemiology predicted a very high probability of population decline over the next 100 years. We believe the modelling approach discussed here is a reasonable description of the disease and its effects on the howler monkey population and can be useful to support evidence-based decision-making to guide actions at a regional level.

Using detection dogs and genetic analyses of scat to expand knowledge and assist felid conservation in Misiones, Argentina.

Many carnivores require large ranges to meet their ecological and energetic needs; however, anthropogenic changes threaten species and their habitats. Camera traps have been used to effectively collect data on carnivores in a variety of habitat types; however, a single survey effort is typically limited to species that have similar body size, habitat use and movement patterns, and individual identification of animals is not always possible. We evaluated whether scat detection dogs could effectively survey for 4 wide-ranging felids that vary in these characteristics: jaguars (Panthera onca), pumas (Puma concolor), ocelots (Leopardus pardalis) and oncillas (Leopardus tigrinus). From June to October 2009 and May to August 2011, a detection dog-handler team detected 588 scats, from which 176 unique genotypes were detected. We assigned sex to 84.7% of the genotyped scats and identified 55 individuals multiple times. The effectiveness of these noninvasive techniques (detection dogs and genetic analyses of scat) not only opens the door for additional studies in areas that were previously difficult or impossible with standard survey techniques, but also provides conservationists with a set of tools that overcome some of the limitations associated with the use of camera traps alone.

Impact of yellow fever outbreaks on two howler monkey species (Alouatta guariba clamitans and A. caraya) in Misiones, Argentina.

Two yellow fever outbreaks (YFOs) occurred in northeastern Argentina between November 2007 and October 2008, seriously affecting populations of two howler monkey species: the brown howler Alouatta guariba clamitans and the black howler Alouatta caraya. Both howlers live syntopically in El Piñalito Provincial Park, Misiones, where four groups (36 individuals) were studied since January 2005. The first dead howlers were found on January 20, 2008, in El Piñalito. Systematic searches found 14 dead howlers within the area (12 from the study groups and two from neighboring groups), with only two young seen on January 25, 2008, and none found since up to December 2008. In October 2008, another YFO hit howler monkey populations from El Soberbio, Misiones. Overall, 59 howlers were found dead in Misiones from November 2007 to December 2008. Thanks to the alert of the howler's death in El Piñalito, a prompt human vaccination campaign started in the area. Wild howler monkey populations from both species are in a delicate situation in Misiones, especially the brown howler, an already endangered species in Argentina and endemic to the Atlantic Forest. If we add the recurrence of YFOs to the reduction of suitable habitat to small fragments, it could be only a matter of time until howler populations disappear from the Upper Paraná Atlantic Forest in Misiones.

Are howler monkey species ecologically equivalent? Trophic niche overlap in syntopic Alouatta guariba clamitans and Alouatta caraya.

According to the principle of competitive exclusion, niche differentiation allows the stable coexistence of closely related species. We analyzed dietary profile and diversity, and dietary overlap between syntopic brown howlers (BR; Alouatta guariba clamitans) and black and gold howlers (BLG; A. caraya) in the Atlantic Forest of NE Argentina, with the objective of evaluating the degree of trophic niche overlap and potential interspecific competition for food. During 12 months, we collected data on feeding behavior of two groups of each howler species using the scan sampling method, together with data on food availability. Both at the group- and species-level, we analyzed feeding behavior in terms of monthly percentages of time spent feeding on each food type and specific food item, dietary diversity (Shannon index H'), and we estimated dietary overlap using the percentage index and the Morisita-Horn index (C(H)). Across months, both howlers showed species-specific preferences for certain food items, and BLG had a more diverse diet (mean+/-SE, H'=2.77+/-0.08) than BR (H'=2.39+/-0.09). However, diets of both species overlapped extensively (percentage index=45.64+/-2.97%; C(H)=0.6+/-0.05) and diets of conspecific groups did not overlap more than diets of groups of different species. Given their high degree of trophic overlap, syntopic BR and BLG meet one of the conditions necessary for interspecific food competition to occur. Although at present we lack direct evidence for interspecific competition in these howler species, we conclude that high levels of niche overlap may have an important role in maintaining the essentially parapatric distribution of howler species throughout the Neotropics.

Infant hybrids in a newly formed mixed-species group of howler monkeys (Alouatta guariba clamitans and Alouatta caraya) in northeastern Argentina.

Natural hybridisation between species has been reported in several primate taxa. In the Neotropics, there is increasing evidence of this phenomenon in howler monkeys (genus Alouatta) in contact zones between species. We describe the first known case of formation of a mixed-species group, and two cases of putative infant hybrids between the brown howler (Alouatta guariba clamitans) and the black howler (A. caraya) in Misiones, Argentina. For 2 years, we followed a group consisting of one adult male and two adult female brown howlers and one adult female black howler. The adult female black howler was observed to copulate twice with brown howler males, and never with black howler males. In December 2006, this female was carrying an infant with a hybrid morphotype. This infant died at approximately 1.5 months of age. In November 2007, the same female had another putative hybrid newborn. This infant male died together with all members of his group during a yellow fever outbreak in early 2008. The lower frequency of mixed-species groups and hybrids at our site compared with other contact zones reported in the literature, suggests that the incidence of natural hybridisation between howler species differs depending on local factors such as population demography and landscape fragmentation.

Allonursing in tufted capuchin monkeys (Cebus nigritus): milk or pacifier?

Allonursing, the behaviour of females nursing offspring that are not their own, is relatively frequent in capuchin monkeys. Using focal-animal sampling and ad libitum observations we describe the pattern of allonursing in a wild group of tufted capuchins, Cebus nigritus (4 cohorts, 22 infants), at Iguazú National Park, north-eastern Argentina, and test several hypotheses on the adaptive value of allonursing. During 2,351 contact hours with the group (including 4,207 focal-animal samples totalizing 329 h focused on infants) we observed 39 allonursing bouts. Infants were not allonursed more frequently by close kin than by more distant allomothers. Offspring of dominant females were allonursed more frequently than those of low-ranking females. Nursing bouts were longer than allonursing bouts. Our results suggest that allonursing in tufted capuchins has a social function and is not mainly aimed at providing milk to infants.